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Genetic Diversity and Phylogenetic Relationships Among Strains of Prevotella (Bacteroides) Ruminicola from the Rumen

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Genetic Diversity and Phylogenetic Relationships Among Strains of Prevotella (Bacteroides) Ruminicola from the Rumen INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1994, p. 246-255 Vol. 44, No. 2 0020-771 3/94/$04.00 +0 Copyright 0 1994, International Union of Microbiological Societies Genetic Diversity and Phylogenetic Relationships among Strains of Prevotella (Bacteroides) ruminicola from the Rumen GORAZD AVGUSTIN,? FRANK WRIGHT,$ AND HARRY J. FLINT* Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB, United Kingdom A high degree of genetic diversity among 29 strains of Prevotella (Bacteroides) ruminicola from the rumen was revealed by comparing restriction fragment length polymorphisms in 16s rRNA genes, sodium dodecyl sulfate-polyacrylamide gel profiles of total-cell proteins, and G+ C contents of chromosomal DNAs. In order to obtain information on phylogenetic relationships, the sequences of a 389-bp region of the 16s rRNA gene, including variable regions 4 and 5, were compared for 10 strains. These 10 strains formed a single group when their sequences were compared with 16s ribosomal DNA sequences from other species, including Bacteroides spp. from the human colon. On the other hand, the great genetic distances between many P. ruminicola strains, including P. ruminicola subsp. brevis B,4 and GA33 and P. ruminicoh 23T (T = type strain), support the hypothesis that these organisms should be reclassified into new species. We identified signature oligonucle- otides based on 16s ribosomal DNA sequences that distinguished strains related to strains 23T, B14, GA33, and M384, as well as an oligonucleotide that specifically recognized all but one of the Bacteroides and Prevotella strains tested. On the basis of the priming activities of these signature oligonucleotides in PCR reactions and on other criteria, we concluded that 12 of the original 29 strains were related to strain 23T, 4 were related to strain B14, and 4 were related to strain GA33. While there are clear grounds for subdividing the species P. ruminicola on the basis of genotypic differences, it is appropriate to delay formal reclassification until further work on the phenotypic differentiation of the new groups is completed. Prevotellu (Bucteroides) ruminicolu has long been recognized distinct species might be represented by these bacteria. In this as one of the most numerous species inhabiting the rumen (5, study we investigated genetic variation in and phylogenetic 20) and can also account for a high proportion of the hind gut relatedness among P. ruminicolu strains of rumen origin. Our microflora of nonruminants, including pigs and humans (18, results fully support previous evidence indicating that there is 30,31). In a recent study, Van Gylswyk (43) found that as many a high degree of genetic divergence among isolates regarded as as 60% of bacterial isolates from rumina of silage-fed cows P. ruminicolu strains and, together with other recent evidence, belonged to this species. The new genus Prevotellu was recently provide the basis for redefining new species within the group. created (37) to distinguish certain former Bucteroides species, including Bucteroides ruminicolu, Bucteroides meluninogenicus, MATERIALS AND METHODS and Bucteroides orulis, from the “true” Bucteroides species more closely related to Bucteroides fragilis. P. ruminicolu has Strains. The bacterial strains which we used and their generally been regarded as a “widely adapted” species. One origins are shown in Table 1. The isolate of strain 23 which we potential role of this organism is in the degradation of plant used gave total-protein sodium dodecyl sulfate (SDS)-poly- cell wall polysaccharides, such as hemicellulose (7, 47) and acrylamide gel electrophoresis (PAGE) profiles identical to pectin (8). P. ruminicolu strains lack a true cellulase system, are the profiles of ATCC 19189 and is the P. ruminicolu type strain. not able to degrade crystalline cellulose, and do not cause M2 medium (17) was prepared anaerobically under 0,-free extensive solubilization of plant cell wall material in pure CO, by using the methods of Bryant (4). cultures. On the other hand, there is evidence that these DNA extraction. The method used to extract chromosomal organisms contribute to plant cell wall degradation by acting DNA was based on a method described by Ausubel et al. (1). synergistically with cellulolytic bacteria (28). In addition, P. Cultures were grown to the stationary phase in M2 broth in ruminicolu strains can generally utilize cellodextrins (32), 100-ml crimp-sealed bottles under anaerobic conditions at starch (6), and a range of soluble sugars. One of their most 38°C. The cells were centrifuged at 4,000 X g for 10 min and significant roles, however, may be in protein and peptide resuspended in 9.5 ml of TE buffer. A 0.5-ml portion of 10% breakdown (26, 44, 45). SDS and 50 pl of a 20-mg/ml proteinase K solution were It has been shown that P. ruminicolu strains exhibit a high added, and the mixture was incubated for 1 h at 37°C. After degree of genetic divergence. Mannarelli et al. (23) found that addition of 1.8 ml of 5 M NaCl and 1.5 ml of a solution the DNA G+C contents of 14 strains varied between 38 and 51 containing 10% hexadecyltrimethyl ammonium bromide in mol%, while 8 strains exhibited less than 30% relatedness with 0.7% NaCl, the mixture was incubated for 20 min at 65°C and the type strain of the species in total DNA-DNA hybridization then extracted with an equal volume of chloroform-isoamyl experiments. These authors concluded that as many as nine alcohol (24:l). Nucleic acids were recovered from the aqueous phase by spooling after precipitation with 0.6 volume of isopropanol and were purified further by CsC1-ethidium bro- * Corresponding author. Mailing address: Rowett Research Insti- mide density gradient centrifugation. The ethidium bromide tute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB, United King- dom. Phone: (0224) 716651. Fax: (0224) 715349. was removed by sequential extraction with water-saturated t Present address: Zootechnical Department, Biotechnical Faculty, n-butanol, samples were dialyzed extensively against TE buffer University of Ljubljana, Groblje 3, 61230 Domiale, Slovenia. at 4”C, and the DNA was concentrated by ethanol precipita- $ Present address: Scottish Agricultural Statistics Service, Edin- tion. burgh EH9 352, United Kingdom. G+C determinations. DNA base compositions (G+C con- 246 VOL.44, 1994 VARIATION AMONG P. RUMINICOLA STRAINS 247 TABLE 1. Origins and characteristics of the 29 P. rurninicola strains examined in this study DNA G+C content PCR amplification with the following signature oligonucleotide primersd:I Overall Origin,, SDS-PAGE 16s ribosomal DNA (mol%)' Strain group restriction pattern This group Previous BacPre 23 GA33 B,4 M384 study studies 23T 1 1 49.2 50.6,' 49.4 + A 118B 1 I ND4 50.6,' 50.9 + A TC18 2 2 46.5 + A TC35 2 2 47.7 + A TC44 2 3 48.9 + A TC27 2 3 47.8 + A TS4-6 2 ND 49.9 + A TF1-10 2 4 ND A TF1-5 2 4 ND A TF1-2 2 4 47.0 + A TC2-3 2 47.7 + A TS 1-2 2 ND + A TC2-24 2 48.9 + A TF2-5 2 47.0 + A GA33T (= ATCC 19188T) 5 ND 50.9.' 50.9 + A FC2 6 5 48.5 A FC4 6 5 48.9 + A FC6 6 ND ND A 223lM217 3 ND 49.1 + B TC2-28 2 50.2 + TS2-7 2 ND 46.3 + 9958178 4 45.3 + TC20 2 44.1 - 2202 7 ND 43Sh + M384 6 42.8 43.8" + B B14 8 3 6 40.7 41.6" + B TC1-1 2 3 6 42.1 + B TF1-3 2 3 6 39.2 + B TS1-5 2 3 39.7 + B '' Strains were grouped as far as possible on the basis of SDS-PAGE and 16s ribosomal DNA data (see text). 1, M. Cotta, US.Department of Agriculture, Peoria, Ill. (5); 2, N. 0. Van Cy swyk, Uppsala, Sweden (43); 3, Rowett Research Institute, Aberdeen, United Kingdom (12); 4, H. N. Shah, London Hospital Medical College, London, United Kingdom; 5, American Type Culture Collection, Rockville, Md.; 6, R. J. Wallace, Rowett Research Institute, Aberdeen, Scotland (26,44); 7, National Collection of Food Bacteria, Shinfield, United Kingdom; 8, J. B. Russell, Cornell University, Ithaca, N.Y. (5). The probable error for DNA G+C content determinations is ? 1%. Strains TC20, 2202, M384, B,4, TC1-1, TF1-3, and TS1-5 have G+C contents that are less than 45 mol%. BacPre, 23, GA33, B,4, and M384 are oligonucleotides that were used as forward primers in PCR; these primers were used together with a universal reverse primer (see Fig. 7). ' Data from reference 23. fData from reference 29. R ND, not determined. Data from reference 22a. tents) were estimated by the thermal denaturation method supplied by Boehringer Mannheim, Mannheim, Germany. (24), using 0.15 M NaC1-0.015 M trisodium citrate and a Unincorporated label was removed by spun column chroma- Gilford model 240 spectrophotometer (38). The DNA base tography, and hybridizations were performed at 65°C as de- ratio was calculated with the following equation: G+C content scribed previously (1 1). = 50.9 + 2.44 (melting temperature of unknown DNA - PCR amplification of 16s ribosomal DNA regions V4 and melting temperature of Escherichia coli DNA). E. coli B DNA V5. Chromosomal DNAs from 10 P. ruminicola strains were was used as the standard. used as target DNAs in PCR reactions by using procedures 16s ribosomal DNA restriction fragment length polymor- described by Sambrook et al. (34). Taq polymerase, reaction phism. Chromosomal DNA was digested to completion with buffers, and deoxyribonucleoside triphosphates were obtained EcoRI (Boehringer Mannheim), and fragments were sepa- from Boehringer Mannheim and were used according to the rated in a 0.6% (wt/vol) agarose gel.
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